Many fishes possess specialized epidermal cells that are ruptured by the teeth of predators, thus reliably indicating the presence of an actively foraging predator. Understanding the evolution of these cells has intrigued evolutionary ecologists because the release of these alarm chemicals is not voluntary. Here, we show that predation pressure does not influence alarm cell production in fishes. Alarm cell production is stimulated by exposure to skin-penetrating pathogens (water moulds: Saprolegnia ferax and Saprolegnia parasitica), skin-penetrating parasites (larval trematodes: Teleorchis sp. and Uvulifer sp.) and correlated with exposure to UV radiation. Suppression of the immune system with environmentally relevant levels of Cd inhibits alarm cell production of fishes challenged with Saprolegnia. These data are the first evidence that alarm substance cells have an immune function against ubiquitous environmental challenges to epidermal integrity. Our results indicate that these specialized cells arose and are maintained by natural selection owing to selfish benefits unrelated to predator-prey interactions. Cell contents released when these cells are damaged in predator attacks have secondarily acquired an ecological role as alarm cues because selection favours receivers to detect and respond adaptively to public information about predation.
In this study we tested whether brook trout (Salvelinus fontinalis) can learn to recognise predators through releaser-induced recognition learning and whether this learning enhances survival of trout during encounters with a predator. In our initial experiment, we exposed hatchery-reared predator-naïve brook trout to chemical stimuli from predatory chain pickerel (Esox niger) paired with alarm signals released by damaged trout, disturbance signals, or distilled water. In subsequent tests 24 h later, when only pickerel odour was presented, trout conditioned with damage-released alarm signals exhibited antipredator behaviour (i.e., decreased movement and altered foraging patterns), in contrast to the other treatments, thereby demonstrating learned recognition of the predator. In our second experiment we showed that trout retained the ability to recognise the predator for at least 10 days. In the next series of experiments we explicitly tested whether training trout to recognise predators confers a survival benefit. During staged encounters with chain pickerel (in both the laboratory and the field), trained fish were better able to evade the predator than nontrained fish. Ours is the first study to demonstrate that fish trained to recognise predators gain a survival benefit during staged encounters with a predator.
Prey animals may mediate the intensity of their behavioural responses to predators to reflect their risk of predation. However, in the absence of an overt (observable) behavioural response to a particular predation-risk cue, we need to ask whether or not prey animals are still using the cue to assess predation risk. Behavioural responses that are not readily observable within the time frame of the experiment are considered covert. In this study we exposed juvenile rainbow trout, Oncorhynchus mykiss, to varying concentrations of conspecific chemical alarm cue to determine their observable response threshold. In a subsequent experiment we exposed the trout to alarm-cue concentrations above and below their behavioural-response threshold and allowed them to interact with an unknown predator (northern pike, Esox lucius). Trout exposed to concentrations below the observable response threshold were able to evade the predator equally as well as trout exposed to alarm-cue concentrations above the observable response threshold. This study illustrates the sophistication with which prey animals employ chemosensory risk assessment. We must use caution when relying on overt behavioural responses for assessing whether prey are utilizing specific cues to mediate their risk of predation.
When fish are exposed to sublethal, environmentally relevant Cu concentrations, olfactory acuity is impaired. The goals of the present study were to investigate the binding dynamics of waterborne Cu in the olfactory epithelium (OE), to examine the influence of calcium (Ca(2+)) on Cu binding, and to link Cu-OE binding to changes in olfactory acuity. Using short-term in vivo waterborne exposures to (64)Cu, we found that Cu accumulates rapidly in the OE, reaching a plateau by 3 h. The binding affinity (log K(Cu-OE)) and binding capacity (B(max)) of (64)Cu in the OE were 6.7 and 10.0 nmol Cu g(-1), respectively. As waterborne Ca(2+) was increased from 50 to 1000 microM L(-1), the B(max) of Cu decreased by approximately 50% while the log K(Cu-OE) remained constant, indicative of noncompetitive inhibition. Using electro-olfactograms (EOG), short-term exposures to 160 and 240 nmol Cu L(-1) were found to reduce olfactory responses to 10(-5) M l-arginine by 72 and 79%, respectively. Short-term exposure to 160 nmol Cu L(-1) also caused a 15-fold reduction in behavioral responses to a food stimulus. Interestingly, increasing waterborne Ca(2+) did not reduce the effects of Cu on EOG or behavioral responses. These results demonstrate that short-term, environmentally realistic concentrations of Cu not only bind to the OE of fathead minnows but also impair their olfactory sensitivity and behavioral responses to olfactory stimuli. Waterborne Ca(2+) reduces Cu-OE binding but does not protect against olfactory impairment.
Predation is one of the most important selective forces acting on prey animals. To respond adaptively to predation threats and increase their chances of survival, prey animals have to be able to recognize their potential predators. Even though a few studies demonstrated innate predator recognition, the vast majority of animals have to rely on learning to acquire this information. Often aquatic prey animals can learn to recognize predators when they detect conspecific alarm cues associated with cues from a novel predator. In this study, we exposed American toad (Bufo americanus) tadpoles to varying concentrations of chemical alarm cues (cues from injured conspecifics). We identified a concentration of cues which caused an overt antipredator response (supra-threshold concentration) and a lower concentration for which the prey failed to exhibit a response (sub-threshold concentration). In a second experiment, we attempted to condition the tadpoles to recognize the odour of larval dragonflies (Anax sp.) by pairing the dragonfly odour with either the sub-threshold concentration or the supra-threshold concentration of alarm cues. In both cases, the tadpoles learned to recognize the predator based on this single pairing of alarm cues and predator odour. Moreover, the intensity of the learned response was stronger for tadpoles conditioned with the supra-threshold concentration of alarm cues than the sub-threshold concentration. This is the first documented case of this mode of learning in anuran amphibians. Learned recognition of predators has important implications for survival.
Mate availability has been shown to influence intrasexual competition and mateguarding behavior across a variety of species. Nevertheless, little is known about how perceived mate scarcity affects such behavior in humans. The purpose of this study was to examine the effects of experimentally induced perceptions of mate availability upon intrasexual competition, jealousy and aggressive mate guarding behavior. Heterosexual undergraduate students (N = 124, 60 women, 64 men) were primed with perceptions of either mate scarcity or mate abundance and subsequently completed measures of intrasexually competitive attitude, jealousy and willingness to aggress against a mate-poacher (either directly or indirectly). For both men and women, results showed that individuals who were exposed to the mate scarcity condition reported significantly more intrasexual competition, jealousy and willingness to aggress indirectly against a matepoacher compared to those exposed to the mate abundance condition. Results provide evidence of an attitudinal and behavioral shift toward sexual conflict when individuals perceive mates to be a scarce resource.
The supposition that prey animals assess and behave flexibly in response to different degrees of predation threat is known as the threat-sensitive predator avoidance hypothesis. We completed a series of field and laboratory experiments to examine whether slimy sculpins (Cottus cognatus) exhibit threat-sensitive predator avoidance when exposed to sympatric predatory brook trout (Salvelinus fontinalis). In a field experiment we caged small and large trout in similar habitats and found that sculpins avoided areas containing trout that were large enough to pose a threat to them, but did not avoid areas containing trout that were small and hence not a threat. In a series of laboratory experiments we found that sculpins showed threat-sensitive predator avoidance when they could assess the predator visually. However, when only chemical cues from the predator were presented, sculpins responded to the predator regardless of its size. Chemical cues seem to function to warn the sculpin that the predator is in the vicinity, but visual cues are needed in order to accurately assess the risk posed by the predator.
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